Parasitism by Cuscuta Pentagona Attenuates Host Plant Defenses Against Insect Herbivores1
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Parasitism by Cuscuta pentagona Attenuates Host Plant Defenses against Insect Herbivores1 Justin B. Runyon, Mark C. Mescher, and Consuelo M. De Moraes* Department of Entomology, Pennsylvania State University, University Park, Pennsylvania 16802 Considerable research has examined plant responses to concurrent attack by herbivores and pathogens, but the effects of attack by parasitic plants, another important class of plant-feeding organisms, on plant defenses against other enemies has not been explored. We investigated how attack by the parasitic plant Cuscuta pentagona impacted tomato (Solanum lycopersicum) defenses against the chewing insect beet armyworm (Spodoptera exigua; BAW). In response to insect feeding, C. pentagona-infested (parasitized) tomato plants produced only one-third of the antiherbivore phytohormone jasmonic acid (JA) produced by unparasitized plants. Similarly, parasitized tomato, in contrast to unparasitized plants, failed to emit herbivore-induced volatiles after 3 d of BAW feeding. Although parasitism impaired antiherbivore defenses, BAW growth was slower on parasitized tomato leaves. Vines of C. pentagona did not translocate JA from BAW-infested plants: amounts of JA in parasite vines grown on caterpillar-fed and control plants were similar. Parasitized plants generally contained more salicylic acid (SA), which can inhibit JA in some systems. Parasitized mutant (NahG) tomato plants deficient in SA produced more JA in response to insect feeding than parasitized wild-type plants, further suggesting cross talk between the SA and JA defense signaling pathways. However, JA induction by BAW was still reduced in parasitized compared to unparasitized NahG, implying that other factors must be involved. We found that parasitized plants were capable of producing induced volatiles when experimentally treated with JA, indicating that resource depletion by the parasite does not fully explain the observed attenuation of volatile response to herbivore feeding. Collectively, these findings show that parasitic plants can have important consequences for host plant defense against herbivores. Plants have evolved the ability to perceive attack proteins that results in systemic acquired resistance to and respond by activating induced defenses (Karban a broad spectrum of pathogens (Durrant and Dong, and Baldwin, 1997; Dangl and Jones, 2001). The de- 2004). However, the categorization of JA as an herbi- fensive strategy utilized is dependent on the attacker vore defense signal and SA as a pathogen defense and can be highly specific. For example, plants can signal is imperfect, as JA-mediated defenses are in- distinguish feeding by closely related herbivore spe- duced by some pathogens and SA-mediated defenses cies and tailor induced volatiles to attract specialist by some herbivores (Moran and Thompson, 2001; parasitoids (De Moraes et al., 1998). The induced phys- Glazebrook, 2005). iological changes of plants in response to herbivores The defenses that plants deploy against one enemy and pathogens are well studied and result from com- may or may not be effective against other enemies plex defense signaling networks regulated by the plant (Stout et al., 2006). Moreover, the JA and SA signaling hormones jasmonic acid (JA) and salicylic acid (SA). In pathways can negatively interact, so that resistance general, the JA pathway is activated in response to to one pest may increase the vulnerability to another. herbivores and regulates production of compounds For example, SA-mediated responses to pathogens that impair digestion (Chen et al., 2005, 2007) and of have been found to negatively affect subsequent JA- induced plant volatiles that attract natural enemies mediated defenses against herbivores, resulting in (Turlings et al., 1990) and repel ovipositing moths (De increased performance of insects that feed on infected Moraes et al., 2001). The SA pathway is typically acti- plants (Felton et al., 1999; Preston et al., 1999; Thaler vated in response to pathogens and mediates a hyper- et al., 1999, 2002; Stout et al., 2006). Although it is well sensitive response and the production of an array of established that SA can inhibit production of JA and antimicrobial phytoalexins and pathogenesis-related the expression of JA-induced defenses (Pen˜a-Corte´s et al., 1993; Doares et al., 1995; Thaler et al., 1999; Cipollini et al., 2004), predicting positive or negative 1 This work was supported by the David and Lucile Packard effects on subsequent enemies has proved difficult Foundation, the DuPont Foundation, and the National Science because a strict dichotomy between the defense path- Foundation (Doctoral Dissertation Improvement grant no. 0608345 ways for pathogen and insect attack does not always and NSF CAREER no. 0643966). exist and the range of organisms affected by each * Corresponding author; e-mail [email protected]. The author responsible for distribution of materials integral to the pathway varies (Felton and Korth, 2000; Thaler et al., findings presented in this article in accordance with the policy 2002, 2004; Cardoza et al., 2003; Stout et al., 2006). described in the Instructions for Authors (www.plantphysiol.org) is: Defense signaling cross talk may allow plants to min- Consuelo M. De Moraes ([email protected]). imize costly, ineffective defenses and fine-tune re- www.plantphysiol.org/cgi/doi/10.1104/pp.107.112219 sponses to specific enemies (Reymond and Farmer, Plant Physiology, March 2008, Vol. 146, pp. 987–995, www.plantphysiol.org Ó 2007 American Society of Plant Biologists 987 Runyon et al. 1998; Kunkel and Brooks, 2002), but the mechanisms talk between the JA and SA pathways, and the avail- underlying JA/SA cross talk are not understood. ability of resources needed for induced defenses. To date, research on induced plant defenses and defense signaling cross talk has focused almost exclu- sively on herbivorous arthropods and pathogens, but RESULTS plants also must defend themselves from attack by Production of JA and SA by Parasitized and other plants. Approximately 4,500 species of flowering Unparasitized Tomato Plants plants (about 1%) are parasitic (Nickrent, 2007) and attach to other plants to obtain water and nutrients To investigate how C. pentagona infestation affected (Kuijt, 1969). Parasitic plants can severely impact host herbivore-induced defenses of the tomato host, we growth and reproduction (Wolswinkel, 1974; Press first constructed a time-course tracking concentrations and Graves, 1995) and have significant effects on the of JA and SA during the first 24 h of BAW feeding structure and productivity of ecosystems in which (Figs. 1 and 2). Amounts of JA began to increase as they occur (Press and Phoenix, 2005; Bardgett et al., soon as 15 min after insect feeding began, and the 2006). Parasitic plants also account for some of the highest JA concentrations occurred after BAW had fed world’s most destructive agricultural pests (Parker for 24 h (Fig. 2A). The production of JA by parasitized and Riches, 1993; Musselman et al., 2001). Dodders, and unparasitized plants was not statistically different genus Cuscuta (Convolvulaceae), are one of the most during the first 2 h of insect feeding, but after 24 h of ecologically and economically significant groups of feeding Cuscuta-infested tomato plants contained only parasitic plants (Kuijt, 1969). Cuscuta spp. have yellow- about 30% of the JA found in unparasitized plants to-orange vines that lack obvious chlorophyll, roots, (mean 6 SE ng/g JA: 278 6 77 parasitized, 812 6 112 and expanded leaves, and thus are completely depen- unparasitized; Fig. 2A). Parasitized and unparasitized dent on aboveground attachment to other plants for control plants, which received no insect feeding, did survival and reproduction (Dawson et al., 1994). We not differ in JA content (Fig. 2A). C. pentagona-infested recently demonstrated that Cuscuta pentagona seed- plants generally contained greater amounts of SA than lings use plant volatiles to locate and choose among unparasitized plants (Fig. 2B), but this difference was hosts (Runyon et al., 2006). Once a host is located, C. not consistently significant due to the large variability pentagona vines twine around the host stem and pro- in SA content in parasitized plants (Fig. 2B). duce haustoria, specialized organs that grow into the host to extract nutrients from both xylem and phloem Production of Herbivore-Induced Volatiles by (Dawson et al., 1994). Cuscuta spp. cause extensive Parasitized and Unparasitized Tomato Plants damage each year to numerous agricultural crops (e.g. tomato [Solanum lycopersicum], alfalfa [Medicago sativa], We next examined the impact of parasitism on host- potato [Solanum tuberosum], soybean [Glycine max], plant volatile production induced by BAW feeding. onion [Allium cepa], and cranberry [Vaccinum macro- carpon]) and, because of their close physiological con- nection to hosts, are difficult to control without also impacting the crop plants (Nadler-Hassar and Rubin, 2003). Despite their economic importance and the profound effects they have on host plants and com- munity dynamics, relatively little is known about the defenses induced by parasitic plant attack or how these defenses affect host plant interactions with other organisms. Trade-offs in plant defenses against different at- tackers are likely central to the ecology and evolution of induced defenses. Moreover, understanding such tradeoffs is key to avoiding unwanted side effects if these pathways are to be manipulated to control pests in agriculture. In this study,